HISTORICAL REVIEW OF THE UNCERTAIN TAXONOMIC STATUS OF CYSTOPTERIS DICKIEANA R.SIM (DICKIE'S BLADDER FERN)

11 Pages·2000·0.29 MB·

by  Dyer, A F

EDINB. J. BOT. 57(1):71–81(2000) 71
HISTORICAL REVIEW OF THE UNCERTAIN
TAXONOMIC STATUS OF CYSTOPTERIS
DICKIEANA R.SIM (DICKIE’S BLADDER FERN)
A. F. DYER*, J. C. PARKS†, AND S. LINDSAY*
Cystopterisdickieana R.Simis arare fernprotectedinBritainunder the 1981Wildlife
and CountrysideAct. Mostcurrentflorastreatitasadistinct species buteversince it
was firstdiscoveredin Scotlandin the1830s,therehasbeen considerable debate about
its taxonomicstatuswithin theC. fragilis complex.This debate centreson therelative
importanceoftwo characters,thearchitecture ofthefronds and thesurface
sculpturingofthe spores,indelimiting C. dickieanafromother taxain theC. fragilis
complex. Thetypespecimens ofC. dickieana havedistinctivefronds.Plantswith
similar frondarchitecturehave, todate,been recordedgrowingnaturallyonly atthe
sitein Scotlandfromwhich the typespecimenswere collectedandatoneother site
nearby. Thetypespecimensof C. dickieanaalso havematuresporeswith surface
sculpturingoften describedas‘rugose’.Theseare distinctiveandunusualin thegenus
Cystopteris,in which mosttaxahave ‘echinate’spores.However, rugose-sporedplants
havebeen recordednotonly at,and near,thetypelocality inScotland butalsoat
manyother sitesinthe northernhemisphere inpopulationsofplants definedlargelyon
the basisoffrondarchitectureas C. fragilis orC. baenitzii.This indicatesthatspore
sculpturingshould notbe usedalone todelimitC. dickieana fromothertaxa withinthe
C. fragilis complexbut,despite this,theliterature on‘C.dickieana’ containsmany
reportsofstudieson materialidentifiedas C. dickieana solelyonthe basisofspore
sculpturing. This,combinedwith the factthatmostcomparative studieshave also
failedtoincludematerial knowntohave comefromthe typelocality,hasresultedin
considerable andcontinuing uncertaintyoverthe taxonomicstatus anddistribution of
C. dickieana.
Keywords. Cystopterisbaenitzii,Cystopterisdentata, Cystopterisfragilis,frond
architecture, sporesculpturing.
INTRODUCTION
Cystopteris dickieana R.Sim is, at present, a fern species protected in Britain under
the 1981 Wildlife and Countryside Act on the basis that it is endemic to Scotland
and extremely rare. However, ever since it was first discovered in the 1830s, there
hasbeenconsiderabledebateaboutitstaxonomicstatuswithintheCystopterisfrag-
ilis complex. Opinions have ranged from acceptance of C. dickieana as a distinct
species endemic to Scotland to: acceptance of C. dickieana as a distinct species but
notendemictoScotlandto:acceptancethatthesametaxonisnomorethanavariety
of the widespread and polymorphic species C. fragilis. It has even been suggested
* RoyalBotanicGardenEdinburgh,20AInverleithRow,EdinburghEH35LR,UK.
† MillersvilleUniversity,POBox1002,Millersville,PA17551–0302,USA.
72 A. F. DYER ET AL.
(though not yet in Britain) that some ‘C. dickieana’ should, in fact, be recognized
as C. baenitzii.
The complexities of the long-running, and continually evolving, debate on C.
dickieana are presented here in the form of an historical review so that the results
of a new investigation on Scottish Cystopteris, recently undertaken at The Royal
Botanic Garden Edinburgh, can be more easily placed in context (see Parks et al.,
2000).
HISTORICAL REVIEW
It [i.e. Cystopteris fragilis] is a plant so polymorphous in character that the species
which botanists have from time to time endeavoured toseparate from it, though some-
times assuming a distinct-looking aspect, appear in other cases to become united by
intermediate forms, and are then with difficulty defined even as varieties. Cystopteris
fragilismustindeedbeconsideredasbeing,likethestillmorepolymorphousAthyrium
filix-foemina and Lastrea dilatata a botanical ignis fatuus, alluring the incautious
novelty-seeker among the quagmires of species-making, in which, at length when his
mental vision becomes cleared by more extended observations, he finds himself hope-
lessly floundering.’ Moore (1859; 258).
‘CystopterisisdominatedbythewidespreadandpolymorphicC.fragiliscomplex,which
constitutes perhaps the most formidable biosystematic problem in the ferns.’ Lovis
(1977: 356).
More than a century after Moore’s comment in 1859, and despite the advent of
biochemical and molecular techniques (Haufler et al., 1990; Haufler & Windham,
1991), the genus Cystopteris as a whole, and C. fragilis in particular, continues to
present difficult problems to fern taxonomists. Of special interest in Scotland is the
statuswithintheC.fragiliscomplexofthefernwidelyknownasCystopterisdickieana
(locally known as ‘Dickie’s bladder fern’), which is one of Scotland’s rarest taxa
and, in the form which characterizes all plants at the type locality (see below),
apparently unique to Scotland.
Cystopteris fragilis (L.) Bernh. is a cosmopolitan polyploid taxon, (Crabbe &
Jermy, 1993; Haufler et al., 1993), which is thought to be of ancient origin because
of the lack of diploids and the worldwide distribution (Lovis, 1977) and because it
acts as a diploid at many of its enzyme loci (Haufler & Windham, 1991).
Chromosome studies reveal that most plants are tetraploid or hexaploid and the
considerablemorphologicalandallozymalvariationindicatesthatthereisevolution-
ary divergence in these polyploids.
Cystopteris dickieanaR.Sim isataxonwhich haslong beenrecognizedwithin the
C.fragiliscomplex(Marren,1984).Itwasdiscoveredinthe1830sbyWilliamKnight
(Dickie,1860). The earliest published reference to it was under the name C. fragilis
(Dickie, 1838) but the description of its habitat makes it clear that Dickie was
THE UNCERTAIN TAXONOMIC STATUS OF CYSTOPTERIS DICKIEANA R.SIM. 73
referring to what is now the type material of C.dickieana. The type specimens were
collected fromaseacave atCove,afew milessouthof Aberdeen,Scotland,in1842
by George Dickie and are now in the herbaria of the Natural History Museum
London(BM)andtheRoyalBotanicGardensKew(K).Thetypelocalityhasbeen
described in detail by Marren (1984). Living material was sent to several people
includingRobertSim,anurserymaninKent,England,whowrotethefirstpublished
description of the plant (Sim, 1848). He placed it in a new taxon, Cystopteris
Dickieana,addingthat‘Ifanyoftherecordedspecies[i.e.thetaxarecognizedwithin
the C. fragilis complex in Britain at that time] apart from C. fragilis have a claim
torankassuch,soalsomustC.Dickieana’.Thefirstpublishedillustration,thistime
as C. fragilis var. Dickieana, appeared a year later (Moore, 1849a) and a more
detaileddescriptionappearedthesameyear(Moore,1849b).Anearlyandimportant
illustration appeared in 1859 (Moore, 1859). It was produced by Henry Bradbury’s
Nature Printing method whereby each print was taken from a copper replica of an
impression made by an actual specimen on a polished lead sheet. No drawing or
engraving was involved, so the print is completely accurate in all details (Fig.1).
Moore firstcultivatedplants from thecave in 1846 and, having proved veryeasy to
grow,ithasbeenincultivationeversince.Itwascollectedinquantitybynurserymen
for resale in the early 1850s. James Backhouse from Yorkshire visited the site in
August 1852 (Backhouse, 1852) and collected herbarium specimens (Fig.2) and
live plants.
Inthe150yearssinceitwasformallydescribed,therehasbeenacontinuingdebate
about the proper taxonomic status of ‘Cystopteris dickieana’ but there has been no
recent review of the history of this debate. Johnson and Sowerby (1855) called the
type material C. Dickieana but referred to it as a variety. Moore published it as a
variety of C. fragilis but, according to Sowerby and Johnson, remarked that ‘I am
inclined to think C. dentata [one of the taxa then recognized within the C. fragilis
complex in Britain; see Fig.1] to be sufficiently distinct to take rank as a species,
and to look upon C. Dickieana as an extreme form of it’. Newman included it as a
species,C.DickieanaSim,inthe1854editionofhisbook,AHistoryofBritishFerns
(Newman, 1854), but stated ‘My own judgement, improved but by no means
matured,bytheobservationsofsixteenyears,regardsdentataasanonentity,angus-
tata asa synonymeof that nonentity,and Dickieanaasa possible, butbyno means
established,species.’Hebasedhisdoubtsaboutitsspecificstatuson‘first,thepresent
restriction of the species to a single locality, and that a very peculiar one; and,
secondly,theabsenceofanyobviouscharacterwherebyitmaybedistinguishedfrom
C. fragilis.’. Most later 19th-century authors favoured varietal or subspecific status
for material from the type locality but it has been accorded species rank in most of
themorerecentBritishfloras,fieldguidesandotherpublications(e.g.Manton,1950;
Clapham et al., 1952; Page, 1988; Jermy & Camus, 1991; Hutchinson & Thomas,
1996; Page, 1997; Stace, 1997), though frequently accompanied by an indication of
the uncertainty regarding its status. Lovis (1977), obviously referring to the type
material, stated: ‘Modern European taxonomic practice accepts Cystopteris dickie-
74 A. F. DYER ET AL.
THE UNCERTAIN TAXONOMIC STATUS OF CYSTOPTERIS DICKIEANA R.SIM. 75
ana,whichpossessesdistinctivemorphologicalfeaturesotherthanitshighlycharac-
teristic spores, as a valid species related to but distinct from C. fragilis.’. It is
apparentlythecombinationofuniquefrondarchitectureanddistinctivelysculptured
spores that encourages this recognition as a separate species but it is worth noting
that other equally extreme frond architectures exist within the C. fragilis complex.
Although many of these have, at some point in the past, also been recognized as
distinct taxa, only two are occasionally recognized in Britain today and then only
as varieties of C. fragilis: C. fragilis (L.) Bernh. var. alpina Hook., and C. fragilis
(L.) Bernh. var. dentata Hook., (Tennant, 1995).
As indicated in Sim’s original description and illustrated by Moore (see drawings
in Fig.1), typical C. dickieana has rugose and minutely verrucate spores (also
describedintheliteratureasrugose,rugate,verrucose,verrucate,ortuberculate,and
here subsequently referred to as ‘rugose’), which is a distinctive feature within
Cystopteris.MostCystopteristaxa,includingmostvariantsofC.fragilis,haveechin-
ate spores (also described in the literature as spiny, spinulose, or spinose and here
subsequently referred to as ‘echinate’), (Blasdell, 1963; Pearman, 1976; Tryon &
Lugardon, 1991). However,as earlyas1855, Johnsonand Sowerbyrecognized that
other variants of ‘C. dentata’ (considered by them as a species but now included in
C. fragilis) also had non-echinate spores. In 1891, C.baenitzii Do¨rfl., reportedfrom
Scandinavia to Siberia but said to be rare in Western Europe, was described from
Norwegian type material as a species distinct from C. fragilis solely on account of
itsnon-echinatespores(Manton,1950).Hagenah(1961)observedplantswith‘non-
spiny’ spores thatotherwise fittedthe descriptionof C.fragilis var.fragilisin North
America. Pearman (1976) reported spores with modifiedspines or no spinesin four
species, includingsomeidentifiedasC.fragilis. Tennant (1995)described somewhat
intermediate, ‘tuberculate’, spores in C. fragilis var. alpina from Teesdale, England.
Non-echinate spores are thus not unique to the type material of C. dickieana and
occur elsewhere within the C. fragilis complex as well as in other species. Rich &
Jermy (1998) concluded that the rugose surface of the spores of C. dickieana is a
character‘oflittletaxonomicsignificance’.Nevertheless,thedelimitationofC.dickie-
ana from C. fragilis has sometimes been reduced to the one character: the presence
of rugose spores (e.g. Blasdell, 1963; Profumo, 1965, 1969; Vida, 1974; Pearman,
1976; Wang, 1983; Prada, 1986; Roa et al., 1988; Fraser-Jenkins, 1997). This has
resulted in reports of C. dickieana from elsewhere in Britain (Tennant, 1996; Jermy
& Harper, 1971) as well as from a wide area of Europe, and from North Africa,
FIG. 1. PlateCIIfromMoore(1859)includingoneoftheearliestpublishedillustrationsof
C. dickieana(herereferredtoas C.fragilis var.dickieana).Theillustration isaNaturePrint
taken from an actual specimen. Scale bar=10cm. Note that the taxa referred to as var.
angustata, var. decurrens and var. interrupta are not recognised in any modern taxonomic
treatment oftheC. fragilis complex.
76 A. F. DYER ET AL.
FIG. 2. Photocopy of a herbarium specimen (at E) of C. dickieana collected at the type
locality by JamesBackhouse SeniorinAugust 1852.Scalebar=10cm.
India, Pakistan, China, Greenland and North America (e.g. Profumo, 1965, 1969;
Nardi, 1974; Pearman, 1976; Vida & Mohay, 1980; Wang, 1983; Prada, 1986;
Labatut, 1988; Roa et al., 1988; Haufler & Windham, 1991; Berg, 1992; Nakaike &
THE UNCERTAIN TAXONOMIC STATUS OF CYSTOPTERIS DICKIEANA R.SIM. 77
Malik, 1992, 1993; Crabbe & Jermy, 1993; Øllgaard & Tind, 1993; Fraser-Jenkins,
1997).
AsemphasizedbyLovis(1977),theplantsusedtotypifyC.dickieanahaveasuite
ofmorphologicalcharactersthat,alongwithrugosespores,aredistinctive(Newman,
1854; Page, 1997). Above a short stipe, the pinnae are oblique to the plane of the
leaf. They are less finely dissected than in C. fragilis, with broad, bluntly rounded
ultimate segments, and crowded on the rachis so that they overlap, and they have
crisped margins. A reviewof the literature reveals that when those who have recog-
nizedC.dickieanaonthebasisofrugosesporesalonehavealsoprovideddescriptions
of frond architecture (e.g. Nardi,1974; Haufler & Windham, 1991; Berg, 1992;
Øllgaard & Tind, 1993;Tennant, 1996;Fraser-Jenkins, 1997), the plants theyident-
ifiedasC.dickieanawereoftenunlikethetypematerialofthatspeciesandfellwithin
the wide range of variation found within C. fragilis and its varieties. So-called ‘C.
dickieana’,indistinguishablefromC.fragilisapartfromthespores,canevenbefound
growingtogetherinthesamepopulationsasplantsthathaveechinatespores(Haufler
& Windham, 1991; Berg, 1992; Øllgaard & Tind, 1993). Hagenah (1961) described
eightinstanceswhere,inasurveyofherbariumcollectionsofNorthAmericanspeci-
mens, he had found some individuals with echinate spores and some with rugose
spores among plants identified as C. fragilis with the same collection number and
presumably therefore from the same population. Where plants producing either
echinate or rugose spores occur close together, plants producing intermediate spore
types have been reported (Øllgaard & Tind, 1993).
Nardi (1974) and Labatut (1988) divided ‘C. dickieana s.l.’ with rugose spores
into ‘C. dickieana s.str.’ and a group related to C. baenitzii Do¨rfl on the basis of a
number of spore and frond characters. However, C. dickieana s.str. as defined by
them still includes plants from Spain, Sicily, and Sardinia that are otherwise more
similar to C. fragilis than to the type material of C. dickieana. Øllgaard and Tind
(1993) expressed concern over the application of the name C. dickieana to
Scandinavian plants with rugosespores butfragilis-like frondsand suggested thatit
might be more appropriate to call these C. baenitzii. Crabbe and Jermy (1993)
included C. baenitzii as a synonym of C. dickieana, with the Scottish type material
ofC.dickieanaasanextremevariantofthespecies.Prada(pers.comm.)alsotreated
C. baenitzii as a synonym of C. dickieana for plants with rugose spores resembling
C. fragilis in frond architecture. Page (1997) has suggested that these plants might
be the product of introgression between the typical C. dickieana and typical C.
fragilis. Fraser-Jenkins (1997) included all these plants within C. fragilis subsp.
dickieana but uniquely considered that the plants fitting the type description for C.
dickieana and now in garden-cultivation should be treated as a cultivar, C. fragilis
(L.) Bernh. subsp. dickieana (R.Sim) Hyl. ‘Dickie’ Fraser-Jenk.
ThewidespreaduseofthebroaderdefinitionofC.dickieana,basedsolelyonspore
sculpturing while ignoring the overlap with C. fragilis in frond architecture, has led
to furtherconfusion.Thus,itdoes notnecessarilyfollowthat statementsbyvarious
authors about C. dickieana are valid for material from the type locality which may
not even have been included in their investigations.
78 A. F. DYER ET AL.
StatementsaboutthedistributionofC.dickieana,asrecognizedbysporescupltur-
ing, hide the fact that, with the possible exception of a plant from Arran, Ireland,
mentioned but not described in detail by Moore (1859), plants with frond architec-
ture fitting the type description of C. dickieana have been found only at, and close
to, the type locality. There are no substantiated reports of such plants at any other
locality within or outside Britain. In a study of the North American distribution of
Cystopteris with ‘non-spiny’ spores, based on light-microscopy, Hagenah (1961)
argued against the recognition of either C.dickieana or C. baenitzii as distinct from
C.fragilisvar.fragilis,andconcludedthat‘therecognitionofspeciesonthegrounds
of spore sculpturing alone does notseem justifiable atthis time’. Blasdell (1963), in
a monograph consideredtobean inadequatetreatment byLovis (1977),concluded
thatC.dickieanawas ‘worthyonlyofdesignationasasporeformwithinC.fragilis’
and included it, with C. baenitzii, under C. fragilis var. fragilis. However, again it
appears that no British material was included in the survey. By contrast, in a later
electron microscopy study of spore morphology, Pearman (1976) recognized C.
fragilis var. dickieana but once more the decision was taken without examining the
type material or more recent collections from the type locality.
C. dickieana in the form which characterizes the type locality is tetraploid
(Manton,1950).However,Manton&Reichstein(1965)andVida&Mohay(1980)
reported hexaploid plants with non-echinate spores from USA, Greenland and the
Swiss Alps and concluded that C. dickieana includes at least two cytotypes. Roa
et al.(1988) and Profumo(1969) stated that there wereno significant differences in
gametophytemorphologybetweenC.dickieanaandC.fragilisbutexaminedgameto-
phytes raised from plants of C. dickieana identified solely on the basis of spore
sculpturingandonlyfromSpainandItalyrespectively;theydidnotincludematerial
from the type locality. Comparisons of isozyme banding patterns (Haufler &
Windham,1991)thatcontributedtotheconclusionthatC.dickieanawasnotdistinct
from C. fragilis were based entirely on North American material in which only the
spore sculpturing consistently separated the two groups. Manton and Reichstein
(1965) reported that a plant that they presumed to be a hybrid between tetraploid
C. fragilis and tetraploid C. dickieana was sterile, reinforcing their decision to attri-
butethemtodifferentspeciesoratleastsubspecies,buttheplantswerefromNorway
(so it was presumably C. dickieana s. l., with fragilis frond architecture and rugose
spores)andagainmaterialfromthetypelocalitywasnotstudied.Bycontrast, Vida
(1974)usedonlymaterialfromthetypelocalityofC.dickieanainagenomeanalysis
ofC.dickieanaandexaminedasynthetichybridbetweenthisandC.fragilisofPolish
origin. He did not comment directly on the spore sculpturing of the parent plants
butpresumablytheywererugoseandechinaterespectively.Heconcludedthatthese
two tetraploids were genomically distinct allopolyploids with only one genome in
common (i.e. YYZZ and XXYY). However, an observed excess of bivalents over
the 42 expected in the hybrid XYYZ if only the Y genomes paired suggests that
genomes X and Z are also related, even in these two widely separated populations.
Vida did not study the relationship of the type C. dickieana with C. fragilis from
THE UNCERTAIN TAXONOMIC STATUS OF CYSTOPTERIS DICKIEANA R.SIM. 79
Britain, which may be more closely related to the type than is the Polish material.
Lovis (1977) reviewed Vida’s cytological evidence and concluded that C. dickieana
was probably a segmental allopolyploid (i.e. YYY∞Y∞).
Asageneralization,overthelast50yearsorso,mostofthosewhohaveconferred
specific status upon C. dickieana have included type material or material known to
have come from the type locality in their investigations. Most of those who favour
synonymy of C. dickieana with C. fragilis, either unnamed (e.g. Blasdell, 1963), or
asavariety[C.fragilis(L.)Bernh.var.dickieana(Sim.)Lindberg.,Medd.Soc.Fauna
etFloraFennica32:21–24.(1905)]orasubspecies[C.fragilissubsp.dickieana(Sim)
Hylander,UppsalaUniv.Arsskr.1945(7):59.(1945)]havenotincludedtypematerial
ormaterialknowntohavecomefromthetypelocalityintheirinvestigations.Thus,
mostofthecurrentfernflorasandfieldguidescoveringScotland(Stace,1997;Page,
1997;Crabbe&Jermy1993;Jermy&Camus,1991)refertoC.dickieanaasadistinct
species, albeit with some reservations.
In conclusion,the taxonomicstatusofC.dickieanawithin theC.fragiliscomplex
remains uncertain and controversial. Indeed, 140 years after Moore’s reference to
the ‘quagmires of species making’, the two basic taxonomic questions regarding C.
dickieana still remain: 1, are all the members of the C. fragilis complex that have
rugosespores members ofthe same taxonasthetype material ofC.dickieana?; and
2, is the type material of C. dickieana a distinct species or a variety/subspecies of
C. fragilis?
ACKNOWLEDGEMENTS
We thank Dr Chris Haufler for helpful comments on an earlier draft of this paper
and Drs Clive Stace and Elizabeth Sheffield for their insightful reviews.
REFERENCES
BACKHOUSE, J. (1852).Cystopteris dickieana.(In anextractfroma letterto The
PhytologistClubpublished intheir Proceedings.)Phytologist 4:716.
BERG, R. Y. (1992).Sporevariasjoniskandinaviskepopulasjonerav Cystopterisfragilis.
Blyttia4: 143–157 [in Norwegian,with English abstract].
BLASDELL, R. F. (1963).A monographicstudyofthe ferngenusCystopteris.
Mem.TorreyBot.Club 21:1–102.
CLAPHAM, A. R., TUTIN, T. G. & WARBURG, E. F. (1952).Floraofthe
British Isles.Cambridge: CambridgeUniversity Press.
CRABBE, J. A. & JERMY, A. C. (1993).Cystopteris. In:TUTIN,T. G.,BURGESS,
N. A.,CHATER, A.O. etal. (eds),FloraEuropea,Vol.1,2nd edition,pp.24–25.
Cambridge: CambridgeUniversity Press.
DICKIE, G. (1838).FloraAberdonensis.Aberdeen:Gray.
DICKIE, G. (1860).Botanist’s GuidetotheFloraofAberdeen, Banffand Kincardine.
Aberdeen:Brown.
FRASER-JENKINS, C. R. (1997).New SpeciesSyndromein IndianPteridology and
the Ferns ofNepal.DehraDun:R.P. S.Gahlot.
80 A. F. DYER ET AL.
HAGENAH, D. J. (1961).Spore studiesinthe genusCystopteris.I. The distributionof
Cystopteriswith non-spinysporesinN. America.Rhodora 63:181–193.
HAUFLER, C. H. & WINDHAM, M. D. (1991).New SpeciesofNorthAmerican
Cystopterisand Polypodium withcommentson theirreticulate relationships.Amer. Fern
J.81: 7–23.
HAUFLER, C. H., WINDHAM, M. D. & RANKER, T. A. (1990).
Biosystematic analysisoftheCystopteristennesseensis (Dryopteridaceae)complex. Ann.
MissouriBot.Gard.77: 314–329.
HAUFLER, C. H., MORAN, R. C., & WINDHAM, M. D. (1993).Cystopteris.
In:MORIN,N. R.(convening ed.) Flora ofNorthAmerica,Vol.2, Pteridophytesand
Gymnosperms,pp.263–270.
HUTCHINSON, G. & THOMAS, B. A. (1996).WelshFerns.Cardiff:National
MuseumofWales.
JERMY, C. & CAMUS, J. (1991).The IllustratedFieldGuide toFernsand Allied
Plantsofthe BritishIsles. London:NaturalHistory Museum.
JERMY, A. C. & HARPER, K. (1971).Spore morphologyofthe Cystopterisfragilis
complex. Brit.Fern Gaz.10: 211–213.
JOHNSON, C. & SOWERBY, J. E. (1855).The Ferns ofGreatBritain.London:
Sowerby.
LABATUT, A. (1988).A proposdeCystopteris dickieanaR.Sim dansl’Herault (France)
etle Valais (Suisse).Bull. Soc.Bot.Centre-Ouest,NS19: 97–100.
LOVIS, J. D. (1977).Evolutionary patternsandprocesses inferns.Adv. Bot.Res.4:
229–415.
MANTON, I. (1950). ProblemsofCytologyand Evolutionin the Pteridophytes.
Cambridge: CambridgeUniversity Press.
MANTON, I. & REICHSTEIN, T. (1965).Diechromosomenzahlen von Cystopteris
sudeticaA.Br.et MildevonBerchtesgarden (Bayern)sowie vonCystopterisdickieana Sim
s.l.vom Foostock(KantonGlarus,Schweiz).Bauhinia 2:307–312.
MARREN, P. (1984).Thehistory ofDickie’s ferninKincardineshire. Pteridologist1:
27–32.
MOORE, T. (1849a).Handbook ofBritish Ferns. London: Warne andRoutledge.
MOORE, T. (1849b).DrDickie’sCystopteris. Bot.Gaz.I: 310–312.
MOORE, T. (1859).NaturePrinted BritishFerns, Vol.2.London: Bradburyand Evans.
NAKAIKE, T. & MALIK, S. (1992).A listofpteridophytes collectedfromPakistan
in1990. In:NAKAIKE,T. & MALIK,S.(eds) CryptogamicFloraof Pakistan, Vol.1,
pp.261–316.Tokyo:NationalScience Museum.
NAKAIKE, T. & MALIK, S. (1993).A listofpteridophytes collectedfromPakistan
in1991. In:NAKAIKE,T. & MALIK,S.(eds) CryptogamicFloraof Pakistan, Vol.2,
pp.317–359.Tokyo:NationalScience Museum.
NARDI, E. (1974).Problemi sistematici edistributivi di‘Cystopteris dickieana’s.l. in
Italia. Webbia 29:329–360.
NEWMAN, E. (1854).AHistory ofBritish Ferns. London:John vanVoorst.
ØLLGAARD, B. & TIND, K. (1993).ScandinavianFerns.Rhodos.
PAGE, C. N. (1988) ANaturalHistory ofBritish Ferns. London: Collins.
PAGE, C. N. (1997).TheFernsofBritainand Ireland, 2ndedition. Cambridge:
Cambridge UniversityPress.
PARKS, J. C., DYER, A. F. & LINDSAY, S. (2000).Allozyme, sporeand frond
variationinsomeScottish populationsofthe fernsCystopterisdickieana andCystopteris
fragilis.Edinb.J.Bot.57 (1): 83–105.
PEARMAN, R. M. (1976).Ascanning electronmicroscopic investigationofthespores
ofthe genusCystopteris. Brit. Fern Gaz.11: 221–230.